Description of the immature stages of Kuwanina

Zootaxa 3926 (4): 576–584
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Article
ISSN 1175-5326 (print edition)
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http://dx.doi.org/10.11646/zootaxa.3926.4.7
http://zoobank.org/urn:lsid:zoobank.org:pub:1FAC6FC6-4336-4D89-B3FC-2F256009C7D7
Description of the immature stages of Kuwanina betula Wu & Liu,
with a discussion of its placement in the Acanthococcidae family group
(Hemiptera: Coccoidea)
SAN-AN WU1 & NAN NAN
The Key Laboratory for Silviculture and Conservation of Ministry of Education, Beijing Forestry University, Beijing, China 100083
1
Corresponding author. E-mail: sananwu@bjfu.edu.cn
Abstract
The immature stages of Kuwanina betula Wu & Liu are described and illustrated. Based on morphological and molecular
data (18S and 28S rDNA), it is argued that K. betula is closer to Pseudochermes Nitsche than to Kuwanina Cockerell in
Fernald and so this species is transferred to Pseudochermes as P. betula (Wu & Liu) comb. nov..
Key words: Cryptococcidae, immature stages, new combination.
Introduction
The scale insects (Hemiptera: Sternorrhyncha: Coccoidea) are small, sap-sucking true bugs sister to the
Aphidoidea. The common name, scale insects, refers to the protective cover or “scale” (generally waxy) that is
secreted by many species. Nearly 8000 species in approximately 50 extant and extinct families have been described
in the superfamily and these include many important agricultural pests (Miller & Davidson, 1990) and invasive
species (Miller et al., 2005). In addition, many species exhibit varied endosymbioses (Buchner, 1965; Gruwell et
al., 2005, 2007), diverse sexual systems (Nur, 1980; Normark, 2003; Ross et al., 2010) and sexual dimorphism
(Gullan & Kosztarab, 1997). The Coccoidea are frequently divided into two informal groups, the archaeococcoids
and the neococcoids (reviewed by Gullan & Cook, 2007), with the former usually considered to include 15 extant
families and the latter 18 extant.
However, the relationships of the families within the neococcoids is not well resolved. Almost all authors agree
that the eriococcids are not monophyletic (Cook et al., 2002; Hodgson, 2002; Cook & Gullan, 2004; Gullan &
Cook, 2007; Hodgson & Hardy, 2013). Phylogenetic analysis of 18S data (Cook & Gullan, 2004) recovered four
groups within Eriococcidae; (i) a clade including Beesoniidae, Stictococcidae and the eriococcid taxa
Cylindrococcus Maskell, Eriococcus buxi (Boyer de Fosncolombe), and E. williamsi Danzig, generally referred to
as the BSE clade; (ii) a Gondwanan group comprising Australian and New Zealand taxa; (iii) an acanthococcid
group comprising species allied to Acanthococcus from both the northern and southern hemispheres plus the
Dactylopiidae; and (iv) just Calycicoccus Brain. This paper considers the relationships of Kuwanina betula Wu &
Liu within these groups of “eriococcids”.
The classification of taxa in the superfamily Coccoidea has been based primarily on morphological
characteristics of the adult females. Little work has been done on the immature stages. Preliminary results showed
that the taxonomy of the immature stages is helpful in determining relationships among taxa (Howell & Tippins,
1990), especially for groups with highly modified adult females. The adult female of K. betula was described by
Wu and Liu (2009) based on material collected from Henan Province, China, on Betula albosinensis Burkill
(Betulaceae), and it has reduced antennae and legs. Nan et al. (2013) provided its 18S and 28S rDNA sequences. In
2012, more material, including nymphs, was collected from the Shennongjia Forest Region [31°30′N, 110°10′E],
Hubei Province, and Baiyun Mountain [34°08′N, 112°05′E], Henan Province, also on Betula albosinensis. The
purpose of this paper is to describe the immature stages (first- and second-instar female nymphs) and, based on the
576 Accepted by C. Hodgson: 10 Feb. 2015; published: 9 Mar. 2015
setal collar about 1/3 length of seta and a circular base, distributed in 6 longitudinal rows on dorsum. Disc pores
and ducts absent.
Margin. Bottle-shaped setae, same size as on dorsum, distributed along margin from mesothorax to abdominal
segment VII.
Second-instar female (Fig. 3). Unmounted material. Body oval, about 0.50 mm long, 0.26 mm wide, red,
with many long white wax filaments (each about 2/3 length of body) along its margin.
Mounted material. Body oval, gently tapering to narrow posterior segments, 0.50–0.54 mm long and
0.28–0.33 mm wide. Antennae 3-segmented, short, length of each segment: I, 11–12 μm, II, 7–8 μm, and III, 16–19
μm; segment III with 4 fleshy setae and a pair of coeloconic sensilla. Eyespots present. Clypeolabral shield about 2
times as long as labium; labium 1 segmented, 43–48 μm long, with 6 pairs of setae. Front and mid legs absent, each
hind leg replaced by a sac-like structure, about 36–37 μm long and 17–26 μm wide, with many translucent pores on
ventral surface. Thoracic spiracles: each anterior spiracle with 7–9 disc pores, mainly with 5 loculi but occasionally
with 4 or 7 loculi, and each posterior spiracle with 9–11 quinquelocular pores. Anal ring located at end of body,
14–15 μm in diameter, with 1 outer row of pores and 6 short setae, each about 10 μm long, surrounded by an
inverted U-shaped sclerotized plate bearing 4 pairs of enlarged setae, longest seta up to 12 μm long, shortest about
5–6 μm long; also with 2 enlarged setae, each about 10 μm long behind anal ring and beyond sclerotized plate.
Anal lobes slightly produced, each with a pair of apical setae, dorsal seta about 10 μm long, ventral setae about 7
μm long.
Venter. Ventral setae hair-like, 3–8 μm long, scattered on head and thorax and forming a transverse row on
each abdominal segment except setae on segment VII thicker and longer. Disc-pores mainly with 5 loculi but
occasionally with 4 or 7 loculi, each pore 4 μm in diameter, distributed throughout venter except medially.
Macrotubular ducts (Wu & Liu (2009) described these ducts as invaginated disc pores) of 2 sizes: large ducts, each
about 16 μm long and 7–8 μm wide and with about 14 pores at inner orifice of outer part in a ring around base,
distributed in more or less a single longitudinal row along margin; and smaller ducts, each about 9 μm and 4–5 μm
wide; with 4 pairs near labium.
Dorsum. Dorsal setae stoutly setose, each 2–6 μm long, scattered on head and thorax and forming a transverse
row on each abdominal segment except those on last segment thicker and longer. Disc-pores generally with 5 loculi
but occasionally with 3, 4 or 7 loculi, same size as ventral disc-pores, distributed throughout dorsum, but most
abundant near margin. Macrotubular ducts of 1 size, similar to ventral large ducts, in a longitudinal row along
margin and with a single duct on midline of abdominal segments III–VII.
Biology. This species may be parthenogenetic and ovoviviparous since no second-instar males, prepupae,
pupae or adult males have been detected.
Acknowledgements
We thank Dr.Takumasa (Demian) Kondo and Dr. Chris J. Hodgson for reviewing this manuscript, correcting the
English and giving helpful suggestions. This project was supported by the National Natural Science Foundation of
China (31372151).
References
Borchsenius, N.S. (1950) Mealybugs and Scale Insects of USSR (Coccoidea). Akademii Nauk SSSR, Zoological Institute,
Moscow, 32, 1–250.
Buchner, P. (1965) Endosymbiosis of Animals with Plant-Like Microorganisms. John Wiley & Sons, New York, 909 pp.
Cook, L.G. & Gullan, P.J. (2004) The gall-inducing habit has evolved multiple times among the eriococcid scale insects
(Sternorrhyncha: Coccoidea: Eriococcidae). Biological Journal of the Linnean Society, 83 (4), 441–452.
http://dx.doi.org/10.1111/j.1095-8312.2004.00396.x
Cook, L.G., Gullan, P.J. & Trueman, H.E. (2002) A preliminary phylogeny of the scale insects (Hemiptera: Sternorrhyncha:
Coccoidea) based on nuclear small-subunit ribosomal DNA. Molecular Phylogenetics and Evolution, 25, 43–52.
http://dx.doi.org/10.1016/S1055-7903(02)00248-8
Gruwell, M.E., Von Dohlen, C.D., Patch, K. & Normark, B.B.(2005) Preliminary PCR survey of bacteria associated with scale
insects (Hemiptera: Coccoidea). In: Erkilic, L. & Kaydan, M.B. (Ed.), Proceedings of the X International Symposium on
IMMATURE STAGES OF KUWANINA BETULA
Zootaxa 3926 (4) © 2015 Magnolia Press ·
583
Scale Insect Studies. Held at Plant Protection Research Institute, Adana, Zirai Muscadele Arastirma Enstitusu, Adana,
Turkey, 19–23 April, 2004, pp. 101–116.
Gruwell, M.E., Morse, G.E. & Normark, B.B. (2007) Phylogenetic congruence of armored scale insects (Hemiptera:
Diaspididae) and their primary endosymbionts from the phylum Bacteroidetes. Molecular Phylogenetics and Evolution,
44, 267–280.
http://dx.doi.org/10.1016/j.ympev.2007.01.014
Gullan, P.J. & Kosztarab, M. (1997) Adaptations in scale insects. Annual Review of Entomology, 42, 23–50.
http://dx.doi.org/10.1146/annurev.ento.42.1.23
Gullan, P.J. & Cook, L.G. (2007) Phylogeny and higher classification of the scale insects (Hemiptera: Sternorrhyncha:
Coccoidea). Zootaxa, 1668, 413–425.
Hodgson, C.J. (2002) Preliminary phylogeny of some non-margarodid Coccoidea (Hemiptera) based on adult male characters.
Bollettino di Zoologia Agraria e di Bachicoltura (Milano), 33, 129–137. [2001]
Hodgson, C.J. & Hardy, N.B. (2013) The phylogeny of the superfamily Coccoidea (Hemiptera: Sternorrhyncha) based on the
morphology of extant and extinct macropterous males. Systematic Entomology, 38 (4), 794–804.
http://dx.doi.org/10.1111/syen.12030
Howell, J.O. (1984) Review of recent studies on the utilization of the immatures in the classification and phylogeny of scale
insects. Proceedings of the 10th International Symposium of Central European Entomofaunistics, Budapest, 1983,
328–330.
Howell, J.O. & Tippins, H.H. (1990) 1.1.2.3 The immature stages. In: Rosen, D. (Ed.), Armored Scale Insects, Their Biology,
Natural Enemies and Control. Series title: World Crop Pests. Vol. 4A. Elsevier, Amsterdam, pp. 29–54. [384 pp.]
Kosztarab, M. (1968) Cryptococcidae, a new family of the Coccoidea (Homoptera). Virginia Journal of Science, 19, 12.
Kozár, F. & Konczné Benedicty, Z. (2008) Description of a new genus Hispaniococcus from Spain, and a new Pseudochermes
species from Canary Islands (Hemiptera Coccoidea Eriococcidae Cryptococcidae). Bollettino di Zoologia agraria e di
Bachicoltura, Series II, 40, 247–260.
Kozár, F., Kaydan, M.B., Konczné Benedicty, Z. & Szita, É. (2013) Acanthococcidae and Related Families of the Palaearctic
Region. Plant Protection Institute, Centre for Agricultural Research, Hungarian Academy of Sciences, Budapest, Hungary,
679 pp.
Lin, Y.-P., Kondo, T., Gullan, P. & Cook, L.G. (2013) Delimiting genera of scale insects: molecular and morphological evidence
for synonymising Taiwansaissetia Tao, Wong and Chang with Coccus Linnaeus (Hemiptera: Coccoidea: Coccidae).
Systematic Entomology, 38 (2), 249–264.
http://dx.doi.org/10.1111/j.1365-3113.2012.00664.x
Miller, D.R. & Davidson, J.A. (1990) 3.1.1 A list of the armored scale insect pests. In: Rosen, D. (Ed.), Armored Scale Insects,
Their Biology, Natural Enemies and Control. Series Title: World Crop Pests. Vol. 4B. Elsevier, Amsterdam, the
Netherlands, pp. 299–306. [688 pp.]
Miller, D.R., Miller, G.L., Hodges, G.S. & Davidson, J.A. (2005) Introduced scale insects (Hemiptera: Coccoidea) of the United
States and their impact on U.S. Agriculture. Proceedings of the Entomological Society of Washington, 107, 123–158.
Nan, N., Deng, J. & Wu, S.A. (2013) A new felt scale genus Macroporicoccus gen. n. (Hemiptera: Coccoidea: Eriococcidae)
from China, with a redescription of Macroporicoccus ulmi (Tang & Hao) comb. n. Zootaxa, 3722 (2), 170–182.
http://dx.doi.org/10.11646/zootaxa.3722.2.3
Normark, B.B. (2003) The evolution of alternative genetic systems in insects. Annual Review of Entomology, 48, 397–423.
http://dx.doi.org/10.1146/annurev.ento.48.091801.112703
Nur, U. (1980) Evolution of unusual chromosome systems in scale insects (Coccoidea: Homoptera). In: Blackman, R.L.,
Hewitt, G.M. & Ashburner, M. (Ed.), Insect Cytogenetics, Royal Entomological Society, London, pp. 97–117.
Ross, L., Pen, I. & Shuker, D.M. (2010) Genomic conflict in scale insects: the causes and consequences of bizarre genetic
systems. Biological Reviews, 85, 807–828.
Tang, F.D. & Hao, J.J. (1995) The Margarodidae and Others of China (Homoptera: Coccoidea of Insecta). Chinese
Agricultural Science Technology Press, Beijing, 738 pp.
Williams, D.J. (1985) The British and some other European Eriococcidae (Homoptera: Coccoidea). Bulletin of the British
Museum (Natural History) Entomology Series, 51, 347–393.
Wu, S.A. (2000) Descriptions of male and immature stages of Cryptococcus ulmi Tang et Hao (Homoptera: Coccoidea:
Eriococcidae) with brief notes on its biology. Entomotaxonomia, 22, 251–256.
Wu, S.A. & Wei, X. (2003) Kuwanina parva (Maskell) A newly recorded felted scale from China. Journal of Beijing Forestry
University, 25, 84–85.
Wu, S.A. & Liu, J. (2009) A new species of the genus Kuwanina from China. Acta Zootaxonomica, 34, 221–223.
Wu, S.A., Nan, N., Gullan, P.J. & Deng, J. (2013) The taxonomy of the Japanese oak red scale insect, Kuwania
quercus (Kuwana) (Hemiptera: Coccoidea: Kuwaniidae), with a generic diagnosis, a key to species and description of a
new species from California. Zootaxa, 3630 (2), 291–307.
http://dx.doi.org/10.11646/zootaxa.3630.2.5
Yang, S.P. & Kosztarab, M. (1967) A morphological and taxonomical study on the immature stages of Antonina and of the
related genera (Homoptera: Coccoidea). Research Division Bulletin Virginia Polytechnic Institute and State University,
Blacksburg, 3, 1–73.
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